venomics; toxinology; mass spectrometry; ant; venom; antimicrobial
Abstract :
[en] Background: Advancements in proteomics, including the technological improvement in instrumentation, have turned mass spectrometry into an indispensable tool in the study of venoms and toxins. In addition, the advance of nanoscale liquid chromatography coupled to nanoelectrospray mass spectrometry allows, due to its high sensitivity, the study of venoms from species previously left aside, such as ants. Ant venoms are a complex mixture of compounds used for defense, predation or communication purposes. The venom from Neoponera ants, a genus restricted to Neotropical regions, is known to have cytolytic, hemolytic, antimicrobial and insecticidal activities. Moreover, venoms from several Neoponera species have been compared and differences in their toxicity related to nesting habitat variation were reported. Therefore, the present study aimed to perform a deep peptidomic analysis of Neoponera villosa venom and a comparison of seasonal and nesting habitat variations using high-resolution mass spectrometry.
Methods: Specimens of N. villosa ants were captured in Panga Natural Reserve (Uberlândia, MG, Brazil) from arboreal and ground-dwelling nests during summer and winter time. The venom glands were dissected, pooled and disrupted by ultra-sonic waves. The venom collected from different habitats (arboreal and ground-dwelling) and different seasons (summer and winter) was injected into a nanoACQUITY ULPC hyphened to a Q-Exactive Orbitrap mass spectrometer. The raw data were analyzed using PEAKS 7.
Results: The results showed a molecular diversity of more than 500 peptides among these venoms, mostly in the mass range of 800–4000 Da. Mutations and post-translational modifications were described and differences among the venoms were observed. Part of the peptides matched with ponericins, a well-known antimicrobial peptide family. In addition, smaller fragments related to ponericins were also identified, suggesting that this class of antimicrobial peptide might undergo enzymatic cleavages.
Conclusion: There are substantial differences among the venom of N. villosa ants collected in different seasons and from different nest habitats. The venom composition is affected by climate changes that influence prey availability and predator presence. Clearly, nano-LC-MS boosted the knowledge about ant venom, a rich source of unexplored and promising bioactive compounds.
Disciplines :
Chemistry
Author, co-author :
Cologna, Camila; Université de Liège - ULiège > Chimie > Laboratoire Spectrométrie de Masse - Chimie Biologique
Santos Rodrigues, Renata; School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo,
Jean, Santos; School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo,
De Pauw, Edwin ; Université de Liège - ULiège > Département de chimie (sciences) > Laboratoire de spectrométrie de masse (L.S.M.)
Candiani Arantes, Eliane
Quinton, Loïc ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie biologique
Language :
English
Title :
Peptidomic investigation of Neoponera villosa venom by high-resolution mass spectrometry: seasonal and nesting habitat variations
Publication date :
2018
Journal title :
Journal of Venomous Animals and Toxins including Tropical Diseases
eISSN :
1678-9199
Publisher :
Center for the Study of Venoms and Venomous Animals (CEVAP), Brazil
Favreau P, Menin L, Michalet S, Perret F, Cheneval O, Stöckling M, et al. Mass spectrometry strategies for venom mapping and peptide sequencing from crude venoms: case applications with single arthropod specimen. Toxicon. 2006;47(6):676-87.
Touchard A, Dauvois M, Arguel MJ, Petitclerc F, Leblanc M, Dejean A, et al. Elucidation of the unexplored biodiversity of ant venom peptidomes via MALDI-TOF mass spectrometry and its application for chemotaxonomy. J Proteome. 2014;105:217-31.
Aguiar AP, Deans AR, Engel MS, Forshage M, MJT H, Jennings JT, et al. Order Hymenoptera. In: Zhang, ZQ, editor. Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness (addenda 2013). Zootaxa. 2013;3703:51-62.
Hölldobler B, Wilson EO. The ants. Cambridge: Belknap Press (Harvard University € Press); 1990.
Aili SR, Touchard A, Escoubas P, Padula MP, Orivel J, Dejean A, et al. Diversity of peptide toxins from stinging ant venoms. Toxicon. 2014;92:166-78.
Davies NW, Wiese MD, Brown SG. Characterisation of major peptides in 'jack jumper' ant venom by mass spectrometry. Toxicon. 2004;43(2):173-83.
Yi GB, McClendon D, Desaiah D, Goddard J, Lister A, Moffitt J, et al. Fire ant venom alkaloid, isosolenopsin A, a potent and selective inhibitor of neuronal nitric oxide synthase. Int J Toxicol. 2003;22(2):81-6.
Orivel J, Redeker V, Le Caer JP, Krier F, Revol-Junelles AM, Longeon A, et al. Ponericins, new antibacterial and insecticidal peptides from the venom of the ant Pachycondyla goeldii. J Biol Chem. 2001;276(21):17823-9.
Cologna CT, Cardoso JS, Jourdan E, Degueldre M, Upert G, Gilles N, et al. Peptidomic comparison and characterization of the major components of the venom of the giant ant Dinoponera quadriceps collected in four different areas of Brazil. J Proteome. 2013;94:413-22.
Orivel J, Dejean A. Comparative effect of the venoms of ants of the genus Pachycondyla (Hymenoptera: Ponerinae). Toxicon. 2001;39(2-3):195-201.
Dejean A, Labrière N, Touchard A, Petitclerc F, Roux O. Nesting habits shape feeding preferences and predatory behavior in an ant genus. Naturwissenschaften. 2014;101(4):323-30.
Touchard A, Aili SR, Fox EGP, Escoubas P, Orivel J, Nicholson GM, et al. The biochemical toxin arsenal from ant venoms. Toxins (Basel). 2016;8(1):30.
Schimidt CA, Shattuck SO. The higher classification of the ant subfamily Ponerinae (Hymenoptera: Formicidae), with a review of Ponerine ecology and behavior. Zootaxa. 2014;3817:1-242.
Pessoa WFB, Silva LCC, Dias LO, Delabie JHC, Costa H, Romano CC. Analysis of protein composition and bioactivity of Neoponera villosa venom (Hymenoptera: Formicidae). Int J Mol Sci. 2016;17(4):513.
Escoubas P, Quinton L, Nicholson GM. Venomics: unravelling the complexity of animal venoms with mass spectrometry. J Mass Spectrom. 2008;43(3):279-95.
Oldrati V, Arrell M, Violette A, Perret F, Sprüngli X, Wolfender JL, et al. Advances in venomics. Mol BioSyst. 2016;12(12):3530-43.
Aili SR, Touchard A, Koh JM, Dejean A, Orivel J, Padula MP, et al. Comparisons of protein and peptide complexity in poneroid and formicoid ant venoms. J Proteome Res. 2016;15(9):3039-54.
Aili SR, Touchard A, Petitclerc F, Dejean A, Orivel J, Padula MP, et al. Combined peptidomic and proteomic analysis of electrically stimulated and manually dissected venom from the South American bullet ant Paraponera clavata. J Proteome Res. 2017;16(3):1339-51.
Van Vaerenbergh M, Cardoen D, Formesyn EM, Brunain M, Van DG, Blank S, et al. Extending the honey bee venome with the antimicrobial peptide apidaecin and a protein resembling wasp antigen 5. Insect Mol Biol. 2013;22(2):199-210.
Danneels EL, Van Vaerenbergh M, Debyser G, Devreese B, de Graaf DC. Honeybee venom proteome profile of queens and winter bees as determined by a mass spectrometric approach. Toxins (Basel). 2015;7(11):4468-83.
Nadolski J. Effects of the European hornet (Vespa crabro Linnaeus 1761) crude venom on its own species. J Venom Anim Toxins Incl Trop Dis. 2013;19:4. https://doi.org/10.1186/1678-9199-19-4.
Cook SC, Eubanks MD, Gold RE, Behmer ST. Seasonality directs contrasting food collection behavior and nutrient regulation strategies in ants. PLoS One. 2011;6(9):e25407.
Dejean A, Lachaud JP. Ecology and behavior of the seed-eating ponerine ant Brachyponera senaarensis (Mayr). Insects Soc. 1994;41:191-210.
Leal IR, Oliveira PS. Behavioral ecology of the neotropical termite-hunting ant Pachycondyla (= Termitopone) marginata: colony founding, group-raiding and migratory patterns. Behav Ecol Sociobiol. 1995;37:373-83.
Medeiros FNS, Oliveira PS. Season-dependent foraging patterns: case study of a neotropical forest-dwelling ant (Pachycondyla striata Ponerinae). In: Jarau S, Hrncir M, editors. Food exploitation by social insects: ecological, behavioral, and theoretical approaches. Boca Raton: CRC, Taylor & Francis Group; 2009. p. 81-95.
Camacho GP, Vasconcelos HL. Ants of the Panga Ecological Station, a Cerrado Reserve in Central Brazil. Sociobiology. 2015;62(2):281-95.
Touchard A, Labrière N, Roux O, Petitclerc F, Orivel J, Escoubas P, et al. Venom toxicity and composition in three Pseudomyrmex ant species having different nesting modes. Toxicon. 2014;88:67-76.
Escoubas P, Corzo G, Whiteley BJ, Célérier ML, Nakajima T. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and high-performance liquid chromatography study of quantitative and qualitative variation in tarantula spider venoms. Rapid Commun Mass Spectrom. 2002;16(5):403-13.
Chippaux JP, Williams V, White J. Snake venom variability: methods of study, results and interpretation. Toxicon. 1991;29(11):1279-303.
Verano-Braga T, Dutra AA, León IR, Melo-Braga MN, Roepstorff P, Pimenta AM, et al. Moving pieces in a venomic puzzle: unveiling post-translationally modified toxins from Tityus serrulatus. J Proteome Res. 2013;12(7):3460-70.
Mendes MA, Palma MS. Two new bradykinin-related peptides from the venom of the social wasp Protopolybia exigua (Saussure). Peptides. 2006;27(11):2632-9.
Corzo G, Escoubas P, Villegas E, Barnham KJ, He W, Norton RS, et al. Characterization of unique amphipathic antimicrobial peptides from venom of the scorpion Pandinus imperator. Biochem J. 2001;359(Pt 1):35-45.
Johnson SR, Copello JA, Evans MS, Suarez AV. A biochemical characterization of the major peptides from the venom of the giant neotropical hunting ant Dinoponera australis. Toxicon. 2010;55(4):702-10.
Wang K, Dang W, Yan J, Chen R, Liu X, Yan W, et al. Membrane perturbation action mode and structure-activity relationships of Protonectin, a novel antimicrobial peptide from the venom of the neotropical social wasp Agelaia pallipes pallipes. Antimicrob Agents Chemother. 2013;57(10):4632-9.
